Sea cucumber species of the Merambong Shoal with notes on the distribution and habitat of the dominant species

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Malayan Nature Journal 2014, 66(1and2), 159-167 Sea cucumber species of the Merambong Shoal with notes on the distribution and habitat of the dominant species S.P. WOO, C.P. TEH, M.R. NORHANIS, N. NITHIYAA, P.F. AMELIA-NG, Y. ZULFIGAR AND S.H. TAN Abstract: A study on the diversity and distribution of sea cucumbers was done in the seagrass bed of the Merambong Shoal at the southern tip of Peninsular Malaysia. A total of nine species of sea cucumbers were found in the seagrass bed. Two dominant species were Cercodemas anceps and Colochirus quadrangularis which were found in abundance in the Merambong Shoal. The species C. quardangularis was found to have a close association with the seagrass Enhalus acoroides where C. quadrangularis was only found to be attached on the leave blades concentrated at the north-eastern part of the Merambong shoal. Keywords: seagrass, Holothuroidea, association, Straits of Johor. Marine Science Laboratory, School of Biological Sciences, Universiti Sains Malaysia, 11800 Minden, Penang, Malaysia. E-mail: abe_woo@hotmail.com 159

INTRODUCTION Sea cucumbers can be found in almost all marine environments encompassing the deepest oceanic floor to the shallow coral reefs and intertidal areas. Apart from depth, sea cucumbers were also very versatile in inhabiting different substrates from hard sandy bottom, soft and muddy bottom to seagrasses. The knowledge of diversity and distribution of sea cucumbers in Malaysia is very limited, if not only confined to records of species from the shallow coral reef areas (Hashim & Che Bashah, 1985; Zulfigar et al., 2008; Kamarul, 2010; Woo et al., 2013). Only one record of sea cucumbers associated with a seagrass area was done by Zulfigar et al. (2000) in Pulau Tinggi, east coast of the Peninsular Malaysia whereby this species list is limited to sea cucumber species from a coral reef habitat due to the location of the seagrasses that were situated within the vicinity of a coral reef. Apart from coral reefs, seagrass meadows also serve as one of the important habitats that harbour a large diversity of marine organisms especially sea cucumbers (Zulfigar et al., 2000) that were yet to be reported. MATERIALS AND METHODS A survey of sea cucumbers was done in the seagrass bed of the Merambong Shoal at the southern tip of Peninsular Malaysia as shown in Figure 1. The Merambong Shoal seagrass covers a wide area of over 30 hectares (Bujang & Zakaria, 2003) with a mixture of ten different species of seagrasses (Bujang et al., 2006) making it one of the few areas with the most diverse species of seagrasses in Malaysia. Wandering transect was employed in the survey by walking at the seagrass bed when it was exposed extensively during the best low spring tide of the year. The exposure of the seagrass bed only allows a window of two hours of sampling per day for three days. Sea cucumbers were collected using labelled sampling bags and brought back to the laboratory for further identifications. Observation on the substrates and characteristics of the habitat where the samples were found were noted. Colour photographs of the live samples were taken before preservation. In the laboratory, sea cucumbers were identified to the lowest possible taxonomic level. Identification was performed using the main identification keys of Clark and Rowe (1971). The morphologies of the two most dominant species were described in the following section. All samples were preserved by drying and deposited in Marine Science Laboratory, Universiti Sains Malaysia. 160

RESULT AND DISCUSSION There were a total of nine species of sea cucumber found on the seagrass bed of the Merambong Shoal as shown in Table 1. Two dominant species of sea cucumber were found in the seagrass bed of Merambong Shoal, namely Colochirus quadrangularis and Cercodemas anceps.both of the sea cucumbers were from the same family of Cucumariidae and were not difficult to distinguish due to their conspicuous bright colouration. Colochirus quadrangularis Troschel, 1846: 84; Massin, 1990: 5; Liao, 1996: 8; Puchakarn and Sonchaeng, 2004: 426; Marsh and Morrison, 2004: 329; Lam and Todd, 2013: 200. Holothuria quadrangularis Selenka, 1868: 112; Semper, 1868: 60; Theel, 1882: 121; Bell, 1989: 7; Pearson, 1949: 446; Panning, 1949: 446. Pentacta quadrangularis Clark, 1946; Clark and Rowe, 1971: 180, Pl 26; James 1984. Materials examined: Four specimens collected from the seagrass bed of the Merambong Shoal (Johor, Malaysia), exposed seagrass bed (low spring tide). Description: Shape of body quadrangular with smooth and leathery body surface in the dorsal interambulacral area. Anterior near the oral opening was stout and broader compared to the posterior at the anal opening. Ten dendritic tentacles. Four rows of spiky and hard papillae arranged in a line at the two corners of the dorso-lateral and ventro-lateral areas. Tube feet were arranged in three distinctive lines with clear interambulacra area separating them. Five short papillae surrounded the anal opening. The background colour was reddish yellow especially at the ambulacra area in the dorsal. Tentacles were yellow with reddish endings at the tip (Figure 2). Cercodemas anceps Selenka, 1867 Cercodemas anceps Selenka, 1867; Rowe and Gates, 1995; Puchakarn and Sonchaeng, 2004: 426; Marsh and Morrison, 2004: 329; Pentacta anceps Clark and Rowe, 1971: 180; Maxwell and Cresswell, 1981; Huang et al., 2006 Materials examined: Two specimens collected from the seagrass bed of Merambong Shoal (Johor, Malaysia), exposed seagrass bed (low spring tide). 161

Description: Short and stout body with leathery bumpy body surface. Body was slightly curved upwards. Tentacles were retracted. Two rows of low rising and knobby papillae distributed unevenly around two corners of the dorso-lateral areas. Tube feet were arranged in three distinctive lines with clear interambulacra area separating them. The body background colour was yellow while the tube feet and papillae were red in colour (Figure 3). The seagrasses in the Merambong Shoal exhibit an uneven distribution pattern. There were areas with very dense coverage of seagrasses and some were sparser in distribution with a combination of seaweeds and muddy substrates. One of the most distinctive features was the distribution of one particular species of seagrass (Enhalus acoroides) which was concentrated at the northeast of the intertidal seagrass bed in the Merambong Shoal. This species was not seen at any other place in the entire seagrass bed. Coincidentally, C. quadrangularis was also observed to predominantly populate the northeastern part of the seagrass bed. This species was seen to be always seemingly attached to the long and broad leaves of Enhalus acoroides. The rows of tube feet at the ventral body with suction caps of C. quadrangularis were attached firmly on the surface of the leaves at mid length. Prior to this observation, C. quadrangularis was recorded to be found distributed from the temperate waters of Australia extending to the tropic waters (Rowe and Gates, 1995) as well as in deeper waters (up to 40m) caught by dredging (Marsh and Morrison, 2004). The first observation in the intertidal area was recorded by James (1984) in India. There was no mention of the specific type of substrate where specimens of C. quadrangularis were found in previous records. In the other parts of the seagrass bed, C. quadrangularis was not recorded to be present where the substrate was made out of other species of seagrasses (Halophila spp., Thalassia spp, Syngrodium spp, Cymodocea spp., Halodule spp.) with different compositions. Instead, C. anceps was seen to be able to colonize a greater variety of substrates in the seagrass bed of the Merambong Shoal where they were found throughout the whole area without any distinguishing or apparent types of species and composition of seagrasses. Both species were new records in Malaysian waters and known to be distributed in the Indian Ocean, North Australia, Gulf of Thailand, Philippines to South of Japan (Clark and Rowe, 1971; Putchakarn and Sonchaeng, 2004). Additional samplings were needed to ascertain the seasonality variations and distribution patterns of both species in the seagrass area of the Merambong Shoal. Further investigation on the relationship between the seagrass characteristics and habitat preference of sea cucumbers 162

particularly the two species, can be carried out. ACKNOWLEDGEMENTS We are especially grateful to members of the Marine Science Lab, Universiti Sains Malaysia and Dr. Yuji Ise from University of Tokyo for their kind assistance during the field and laboratory work. We also want to mention the contribution from Universiti Putra Malaysia for sampling and logistic arrangements. This study was in collaboration with the Japan Society for the Promotion of Science for the Asian CORE Program (Coastal Marine Science in Southeast Asia: COMSEA). Special thanks to Dr. Toshihiko Fujita, the leader of Benthos Group (JSPS-COMSEA). We are also grateful for the financial support from the Ministry of Higher Education Malaysia (MOHE) provided through the grant: 304/ PB/650630/U137 163

REFERENCES Bell, F.J. 1884. Echinodermata. In. Report on the zoological collections made in the Indo-Pacific Ocean during the voyage of H.M.S. Alert 1881-82, ed. Coppinger, R.W. London: pp 117 and 509-512. Clark, A.M. 1946. Echinoderms from Australia. Publs. Carnegie Instn. 566: 1-567. Clark, A.M. and Rowe, F.W.E. 1971. Monograph of the shallow-water Indo-West Pacific Echinoderms. London: Trustees of the British Museum (Natural History), pp 171-209. Hashim, R. and Che Bashah, C.C. 1985. Tinjauan awal taburan dan penilaian holothurians di beberapa kawasan perairan Sabah sebagai sumber pemakanan. SUMBER 1: 143-155. Huang, X., Huang, L., Li, Y., Xu, Z., Fong, C.W., Huang, D., Hand, Q., Huang, H., Tan, Y. and Liu, S. 2006. Main seagrass beds and threats to their habitats in the coastal sea of South China. Chinese Science Bulletin 51(2): 136-142. James, D.B. 1984. Studies on Indian Echinoderms- On Psolus mannarensis sp. nov. and Other Dendrochirotids from the Indian Seas. J. Mar. Biol. Ass. India 26(1&2): 109-122. Kamarul, R.K., Aisyah, N.R., Hashim, R. and Usup, G. 2010. An Update on Diversity of Sea Cucumber (Echinodermata: Holothuroidea) in Malaysia. Malayan Nature Journal 62(3):315-334. James, D.B. 1984. Studies on Indian Echinoderms On Psolus mannarensis sp. nov. And other Dendrochirotids from the Indian Seas. J. Mar. Biol. Ass. India 26(1 & 2): 109-122. Lam, K.M. and Todd, P.A. 2013. Spatial differences in subtidal epibiotic community structure in marine at Keppel Bay, Singapore. Nature in Singapore 6: 197-206. Liao, Y. 1998. The Echinoderm fauna of Hauinan Island. In The Marine Biology of the South China Sea: Proceedings of the Third International Conference of the Marine Biology of the South China Sea, ed. Morton, B: Hong Kong University Press, Hong Kong, pp 80. Marsh, L.M. and Morrison, S.M. 2004. Echinoderms of the Dampier Archipelago, Western Australia. Records of the Western Australian Museum Supplement No 6: 293-342. Massin, C. 1990. Holothuroidea of the Rumphius Biohistorical Expedition. Zool. Verh. Leiden 307: 5. Maxwell, J.G.H. and Cresswell, G.R. 1981. Dispersal of tropical marine fauna to the Great Australian Bight by the Leeuwin Current. Australian Journal of Marine and Freshwater Research 32(4): 493-500. Panning, A. 1949. Versuch einer Neuirdnung der Familie Cucumariidae. Zool. Jb. 78: 404-470. Pearson, J. 1910. Marine fauna of Mergui Archipelago. Holothuroid. Proc. Zool. Soc. London: 183-194. Puchakarn, S. and Sonchaeng, P. 2004. Echinoderm fauna of Thailand: History and Inventory Reviews. ScienceAsia 30: 417-428. Rowe, F. W. E., and Gates, J. 1995. Echinodermata. In Zoological Catalogue of Australia 33, ed. Wells, A. Australia: CSIRO, pp 1 510. Selenka, E. 1867. Beitrage zur Anotomie und Systematik der Holothurien. Z. Wiss. Zool 17: 291-374. Semper, C. 1868. Holothurien Reisen im Archipel der Phillippinen 2. Wisssenschaftliche Resultate. Weisbaden. Pp 288. 164

Theel, H. 1882. Report on the Holothuroidea dredged by H.M.S. Challenger during the years 1873-1876. Part 1. Rep. Scient. Results Voy. Challenger (Zool.) 4: 1-176. Troschel, H.F. 1846. Neue Holothurien-Gattungen. Arch. Naturgesch. 1: 60-66. Woo, S.P., Zulfigar, Y., Siti Hasmah, I. And Tan, S.H. 2013. The distribution and diversity of sea cucumbers in the coral reefs of the South China Sea, Sulu Sea and Sulawesi Sea. Deep Sea Research II 96: 13-18. Zulfigar, Y., Sim, Y.K., Tan, S.H. and Shirayama, Y. (2010). Field guide to the Echinoderms (sea cucumber and sea stars) of Malaysia. Japan: Kyoto University Press, pp 1-103. Zulfigar, Y., Tan, S.H., Fujita, T. and Terazaki, M. (2000). The distribution of sea cucumber associated with seagrass beds found in the South China Sea. The 11 th JSPS Joint Seminar on Marine Science, pp 362-368. 165

Table 1. List of species of sea cucumber found in the seagrass bed of the Merambong Shoal. Family Species Cucumariidae Colochirus quadrangularis Troschel, 184 Cercodemas anceps Selenka, 1867 Cucumaria sp1. Cucumaria sp2. Phyllophoridae Globosita murrea Cherbonnier,1988 Caudinidae Acaudina molpadioides (Semper,1867) Holothuriidae Holothuria scabra Jaeger, 1833 Holothuria sp1. Holothuria sp2. Figure 1. Study area in the Merambong Shoal, southern tip of Peninsular Malaysia in the Straits of Johor. 166

Figure 2. Colochirus quadrangularis Figure 3. Cercodemas anceps 167